1932

Abstract

Parasitic plants thrive by infecting other plants. Flowering plants evolved parasitism independently at least 12 times, in all cases developing a unique multicellular organ called the haustorium that forms upon detection of haustorium-inducing factors derived from the host plant. This organ penetrates into the host stem or root and connects to its vasculature, allowing exchange of materials such as water, nutrients, proteins, nucleotides, pathogens, and retrotransposons between the host and the parasite. In this review, we focus on the formation and function of the haustorium in parasitic plants, with a specific emphasis on recent advances in molecular studies of root parasites in the Orobanchaceae and stem parasites in the Convolvulaceae.

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2016-04-29
2024-10-16
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Literature Cited

  1. Aflakpui GKS, Gregory PJ, Froud-Williams RJ. 1.  2005. Carbon (13C) and nitrogen (15N) translocation in a maize-Striga hermonthica association. Exp. Agric. 41:321–33 [Google Scholar]
  2. Akiyama K, Matsuzaki K, Hayashi H. 2.  2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–27 [Google Scholar]
  3. Al-Babili S, Bouwmeester HJ. 3.  2015. Strigolactones, a novel plant hormone. Annu. Rev. Plant Biol. 66:161–86 [Google Scholar]
  4. Alakonya A, Kumar R, Koenig D, Kimura S, Townsley B. 4.  et al. 2012. Interspecific RNA interference of SHOOT MERISTEMLESS-like disrupts Cuscuta pentagona plant parasitism. Plant Cell 24:3153–66 [Google Scholar]
  5. Albrecht H, Yoder JI, Phillips DA. 5.  1999. Flavonoids promote haustoria formation in the root parasite Triphysaria versicolor. Plant Physiol. 119:585–92 [Google Scholar]
  6. Aly R, Cholakh H, Joel DM, Leibman D, Steinitz B. 6.  et al. 2009. Gene silencing of mannose 6-phosphate reductase in the parasitic weed Orobanche aegyptiaca through the production of homologous dsRNA sequences in the host plant. Plant Biotechnol. J. 7:487–98 [Google Scholar]
  7. Aly R, Hamamouch N, Abu-Nassar J, Wolf S, Joel DM. 7.  et al. 2011. Movement of protein and macromolecules between host plants and the parasitic weed Phelipanche aegyptiaca Pers. Plant Cell Rep. 30:2233–41 [Google Scholar]
  8. 8. Angiosperm Phylogeny Group 2009. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG III. Bot. J. Linn. Soc 161:105–21 [Google Scholar]
  9. Asai S, Shirasu K. 9.  2015. Plant cells under siege: plant immune system versus pathogen effectors. Curr. Opin. Plant Biol. 28:1–8 [Google Scholar]
  10. Atsatt PR. 10.  1973. Parasitic flowering plants: How did they evolve?. Am. Nat. 107:502–10 [Google Scholar]
  11. Ayre BG, Keller F, Turgeon R. 11.  2003. Symplastic continuity between companion cells and the translocation stream: Long-distance transport is controlled by retention and retrieval mechanisms in the phloem. Plant Physiol. 131:1518–28 [Google Scholar]
  12. Baidouri ME, Carpentier MC, Cooke R, Gao D, Lasserre E. 12.  et al. 2014. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res. 24:831–38 [Google Scholar]
  13. Baird WV, Riopel JL. 13.  1983. Experimental studies of the attachment of the parasitic angiosperm Agalinis purpurea to a host. Protoplasma 118:206–18 [Google Scholar]
  14. Baird WV, Riopel JL. 14.  1984. Experimental studies of haustorium initiation and early development in Agalinis purpurea (L.) Raf. (Scrophulariaceae). Am. J. Bot. 71:803–14 [Google Scholar]
  15. Baird WV, Riopel JL. 15.  1985. Surface characteristics of root and haustorial hairs of parasitic Scrophulariaceae. Bot. Gaz. 146:63–69 [Google Scholar]
  16. Bandaranayake PCG, Filappova T, Tomilov A, Tomilova NB, Jamison-McClung D. 16.  et al. 2010. A single-electron reducing quinone oxidoreductase is necessary to induce haustorium development in the root parasitic plant Triphysaria. Plant Cell 22:1404–19 [Google Scholar]
  17. Bandaranayake PCG, Tomilov A, Tomilova NB, Ngo QA, Wickett N. 17.  et al. 2012. The TvPirin gene is necessary for haustorium development in the parasitic plant Triphysaria versicolor. Plant Physiol. 158:1046–53 [Google Scholar]
  18. Bandaranayake PCG, Yoder JI. 18.  2013. Haustorium initiation and early development in parasitic Orobanchaceae. See Ref. 68 61–74
  19. Bandaranayake PCG, Yoder JI. 19.  2013. Trans-specific gene silencing of acetyl-CoA carboxylase in a root-parasitic plant. Mol. Plant-Microbe Interact. 26:575–84 [Google Scholar]
  20. Bar-Nun N, Sachs T, Mayer AM. 20.  2008. A role for IAA in the infection of Arabidopsis thaliana by Orobanche aegyptiaca. Ann. Bot. 101:261–65 [Google Scholar]
  21. Barkman TJ, McNeal JR, Lim SH, Coat G, Croom HB. 21.  et al. 2007. Mitochondrial DNA suggests at least 11 origins of parasitism in angiosperms and reveals genomic chimerism in parasitic plants. BMC Evol. Biol. 7:248 [Google Scholar]
  22. Birschwilks M, Haupt S, Hofius D, Neumann S. 22.  2006. Transfer of phloem-mobile substances from the host plants to the holoparasite Cuscuta sp. J. Exp. Bot. 57:911–21 [Google Scholar]
  23. Bortesi L, Fischer R. 23.  2015. The CRISPR/Cas9 system for plant genome editing and beyond. Biotechnol. Adv. 33:41–52 [Google Scholar]
  24. Brotherson JD, Simmons BT, Ball T, Anderson WR. 24.  2005. Nutrient relationships between Orobanche fasciculata Nutt. and its host Artemisia pygmaea Gray in the Uinta Basin of Utah, USA. West. N. Am. Nat. 65:242–47 [Google Scholar]
  25. Chang M, Lynn DG. 25.  1986. The haustorium and the chemistry of host recognition in parasitic angiosperms. J. Chem. Ecol. 12:561–79 [Google Scholar]
  26. Chen QL, Jia YM, Wang ZF, Shan CG, Zhu JB, Guo YH. 26.  2011. Postembryonic development of Cistanche tubulosa (Schrenk) Whigt. Pak. J. Bot. 43:1823–30 [Google Scholar]
  27. Choudhury NK, Sahu D. 27.  1999. Photosynthesis in Cuscuta reflexa: a total plant parasite. Photosynthetica 36:1–9 [Google Scholar]
  28. Conn CE, Bythell-Douglas R, Neumann D, Yoshida S, Whittington B. 28.  et al. 2015. Convergent evolution of strigolactone perception enabled host detection in parasitic plants. Science 349:540–43 [Google Scholar]
  29. Cosgrove DJ. 29.  2000. Loosening of plant cell walls by expansins. Nature 407:321–26 [Google Scholar]
  30. Costea M, Tardif FJ. 30.  2006. The biology of Canadian weeds. 133. Cuscuta campestris Yuncker, C. gronovii Willd. ex Schult., C. umbrosa Beyr. ex Hook., C. epithymum (L.) L. and C. epilinum Weihe. Can. J. Plant Sci. 86:293–316 [Google Scholar]
  31. David-Schwartz R, Runo S, Townsley B, MacHuka J, Sinha N. 31.  2008. Long-distance transport of mRNA via parenchyma cells and phloem across the host-parasite junction in Cuscuta. New Phytol. 179:1133–41 [Google Scholar]
  32. Davis CC, Xi Z. 32.  2015. Horizontal gene transfer in parasitic plants. Curr. Opin. Plant Biol. 26:14–19 [Google Scholar]
  33. Dawson JH, Musselman LJ, Wolswinkel P, Dorr I. 33.  1994. Biology and control of Cuscuta. Rev. Weed Sci. 6:265–317 [Google Scholar]
  34. Dobbin DR, Kuijt J. 34.  1974. Anatomy and fine structure of the mistletoe haustorium (Phthirusa pyrifolia). I. Development of the young haustorium. Am. J. Bot. 61:535–43 [Google Scholar]
  35. Dorr I. 35.  1969. Feinstruktur intrazellular wachsender Cuscuta-Hyphen. Protoplasma 67:123–37 [Google Scholar]
  36. Dorr I. 36.  1997. How Striga parasitizes its host: a TEM and SEM study. Ann. Bot. 79:463–72 [Google Scholar]
  37. Dorr I, Kollmann R. 37.  1995. Symplasmic sieve element continuity between Orobanche and its host. Bot. Acta 108:47–55 [Google Scholar]
  38. Dorr I, Visser JH, Kollmann R. 38.  1979. On the parasitism of Alectra vogelii Benth. (Scrophulariaceae) III. The occurrence of phloem between host and parasite. Z. Pflanzenphysiol. 84:213–22 [Google Scholar]
  39. Estabrook EM, Yoder JI. 39.  1998. Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol. 116:1–7 [Google Scholar]
  40. Fernandez-Aparicio M, Rubiales D, Bandaranayake PC, Yoder JI, Westwood JH. 40.  2011. Transformation and regeneration of the holoparasitic plant Phelipanche aegyptiaca. Plant Methods 7:36 [Google Scholar]
  41. Fisher JP, Phoenix GK, Childs DZ, Press MC, Smith SW. 41.  et al. 2013. Parasitic plant litter input: a novel indirect mechanism influencing plant community structure. New Phytol. 198:222–31 [Google Scholar]
  42. Funk HT, Berg S, Krupinska K, Maier UG, Krause K. 42.  2007. Complete DNA sequences of the plastid genomes of two parasitic flowering plant species, Cuscuta reflexa and Cuscuta gronovii. BMC Plant Biol. 7:45 [Google Scholar]
  43. Geldner N. 43.  2013. Casparian strips. Curr. Biol. 23:R1025–26 [Google Scholar]
  44. Giraldo MC, Valent B. 44.  2013. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11:800–14 [Google Scholar]
  45. Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H. 45.  2012. Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos. Trans. R. Soc. Lond. B 367:1461–68 [Google Scholar]
  46. Goldwasser Y, Plakhine D, Kleifeld Y, Zamski E, Rubin B. 46.  2000. The differential susceptibility of vetch (Vicia spp.) to Orobanche aegyptiaca: anatomical studies. Ann. Bot. 85:257–62 [Google Scholar]
  47. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA. 47.  et al. 2008. Strigolactone inhibition of shoot branching. Nature 455:189–94 [Google Scholar]
  48. Gurney AL, Grimanelli D, Kanampiu F, Hoisington D, Scholes JD, Press MC. 48.  2003. Novel sources of resistance to Striga hermonthica in Tripsacum dactyloides, a wild relative of maize. New Phytol. 160:557–68 [Google Scholar]
  49. Gurney AL, Slate J, Press MC, Scholes JD. 49.  2006. A novel form of resistance in rice to the angiosperm parasite Striga hermonthica. New Phytol. 169:199–208 [Google Scholar]
  50. Harloff HJ, Wegmann K. 50.  1993. Evidence for a mannitol cycle in Orobanche ramosa and Orobanche crenata. J. Plant Physiol. 141:513–20 [Google Scholar]
  51. Haupt S, Oparka KJ, Sauer N, Neumann S. 51.  2001. Macromolecular trafficking between Nicotiana tabacum and the holoparasite Cuscuta reflexa. J. Exp. Bot. 52:173–77 [Google Scholar]
  52. Heide-Jorgensen HS. 52.  1991. Anatomy and ultrastructure of the haustorium of Cassytha pubescens R. Br. I. The adhesive disk. Bot. Gaz. 152:321–34 [Google Scholar]
  53. Heide-Jorgensen HS. 53.  2013. Introduction: the parasitic syndrome in higher plants. See Ref. 68 1–18
  54. Heide-Jorgensen HS, Kuijt J. 54.  1993. Epidermal derivatives as xylem elements and transfer cells—a study of the host-parasite interface in 2 species of Triphysaria (Scrophulariaceae). Protoplasma 174:173–83 [Google Scholar]
  55. Heide-Jorgensen HS, Kuijt J. 55.  1995. The haustorium of the root parasite Triphysaria (Scrophulariaceae), with special reference to xylem bridge ultrastructure. Am. J. Bot. 82:782–97 [Google Scholar]
  56. Heinricher E. 56.  1895. Anatomischer Bau und Leistung der Saugorgane der Schuppenwurz-Arten (Lathraea clandestina Lam. und L. squamaria L.). Beitr. Biol. Pflanz. 7:315–406 [Google Scholar]
  57. Hibberd JM, Quick WP, Press MC, Scholes JD, Jeschke WD. 57.  1999. Solute fluxes from tobacco to the parasitic angiosperm Orobanche cernua and the influence of infection on host carbon and nitrogen relations. Plant Cell Environ. 22:937–47 [Google Scholar]
  58. Honaas LA, Wafula EK, Yang Z, Der JP, Wickett NJ. 58.  et al. 2013. Functional genomics of a generalist parasitic plant: laser microdissection of host-parasite interface reveals host-specific patterns of parasite gene expression. BMC Plant Biol. 13:9 [Google Scholar]
  59. Ichihashi Y, Mutuku JM, Yoshida S, Shirasu K. 59.  2015. Transcriptomics exposes the uniqueness of parasitic plants. Brief. Funct. Genom. 14:275–82 [Google Scholar]
  60. Ikeue D, Schudoma C, Zhang W, Ogata Y, Sakamoto T. 60.  et al. 2015. A bioinformatics approach to distinguish plant parasite and host transcriptomes in interface tissue by classifying RNA-Seq reads. Plant Methods 11:34 [Google Scholar]
  61. Irving LJ, Cameron DD. 61.  2009. You are what you eat: interactions between root parasitic plants and their hosts. Adv. Bot. Res. 50:87–138 [Google Scholar]
  62. Ishida JK, Yoshida S, Ito M, Namba S, Shirasu K. 62.  2011. Agrobacterium rhizogenes-mediated transformation of the parasitic plant Phtheirospermum japonicum. PLOS ONE 6:e25802 [Google Scholar]
  63. Ishida JK, Yoshida S, Watakake T, Takebayashi Y, Kasahara H. 63.  et al. 2016. Local auxin biosynthesis mediated by a YUCCA flavin monooxygenase regulates the haustorium development in the parasitic plant Phtheirospermum japonicum. Submitted Identifies the YUCCA gene, encoding an auxin biosynthesis enzyme, and its importance in haustorium formation in P. japonicum.
  64. Jasmin D, Yoder J. 64.  2001. Heritable variation in quinone-induced haustorium development in the parasitic plant Triphysaria. Plant Physiol. 4:1870–79 [Google Scholar]
  65. Jeon JR, Baldrian P, Murugesan K, Chang YS. 65.  2012. Laccase-catalysed oxidations of naturally occurring phenols: from in vivo biosynthetic pathways to green synthetic applications. Microb. Biotechnol. 5:318–32 [Google Scholar]
  66. Jiang F, Jeschke WD, Hartung W. 66.  2003. Water flows in the parasitic association Rhinanthus minor/Hordeum vulgare. J. Exp. Bot. 54:1985–93 [Google Scholar]
  67. Joel DM. 67.  2013. Functional structure of the mature haustorium. See Ref. 68 25–60
  68. Joel DM, Gressel J, Musselman LJ. 68.  2013. Parasitic Orobanchaceae Heidelberg, Ger: Springer [Google Scholar]
  69. Joel DM, Losnergoshen D. 69.  1994. The attachment organ of the parasitic angiosperms Orobanche cumana and O. aegyptiaca and its development. Can. J. Bot. 72:564–74 [Google Scholar]
  70. Kaiser B, Vogg G, Furst UB, Albert M. 70.  2015. Parasitic plants of the genus Cuscuta and their interaction with susceptible and resistant host plants. Front. Plant Sci. 6:45 [Google Scholar]
  71. Keyes WJ, Palmer AG, Erbil WK, Taylor JV, Apkarian RP. 71.  et al. 2007. Semagenesis and the parasitic angiosperm Striga asiatica. Plant J. 51:707–16 [Google Scholar]
  72. Keyes WJ, Taylor JV, Apkarian RP, Lynn DG. 72.  2001. Dancing together. Social controls in parasitic plant development. Plant Physiol. 127:1508–12 [Google Scholar]
  73. Kim D, Kocz R, Boone L, Keyes WJ, Lynn DG. 73.  1998. On becoming a parasite: evaluating the role of wall oxidases in parasitic plant development. Chem. Biol. 5:103–17 [Google Scholar]
  74. Kim G, LeBlanc M, Wafula EK, Depamphilis CW, Westwood JH. 74.  2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–11Showed that bulk mRNA transfer occurs between hosts and parasites. [Google Scholar]
  75. Kim G, Westwood JH. 75.  2015. Macromolecule exchange in Cuscuta–host plant interactions. Curr. Opin. Plant Biol. 26:20–25 [Google Scholar]
  76. Kirigia D, Runo S, Alakonya A. 76.  2014. A virus-induced gene silencing (VIGS) system for functional genomics in the parasitic plant Striga hermonthica. Plant Methods 10:16 [Google Scholar]
  77. Koltai H. 77.  2014. Receptors, repressors, PINs: a playground for strigolactone signaling. Trends Plant Sci. 19:727–33 [Google Scholar]
  78. Kuijt J. 78.  1969. The Biology of Parasitic Flowering Plants Berkeley: Univ. Calif. Press [Google Scholar]
  79. Kuijt J. 79.  1977. Haustoria of phanerogamic parasites. Annu. Rev. Phytopathol. 15:91–118 [Google Scholar]
  80. Lavenus J, Goh T, Roberts I, Guyomarc'h S, Lucas M. 80.  et al. 2013. Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18:450–58 [Google Scholar]
  81. Leblanc M, Kim G, Patel B, Stromberg V, Westwood J. 81.  2013. Quantification of tomato and Arabidopsis mobile RNAs trafficking into the parasitic plant Cuscuta pentagona. New Phytol. 200:1225–33 [Google Scholar]
  82. Lee KB. 82.  2007. Structure and development of the upper haustorium in the parasitic flowering plant Cuscuta japonica (Convolvulaceae). Am. J. Bot. 94:737–45 [Google Scholar]
  83. Li J, Timko MP. 83.  2009. Gene-for-gene resistance in Striga-cowpea associations. Science 325:1094Identified resistance genes against parasitic plants for the first time. [Google Scholar]
  84. Llugany M, Lombini A, Dinelli E, Poschenrieder C, Barceló J. 84.  2009. Transfer of selected mineral nutrients and trace elements in the host-hemiparasite association, Cistus–Odontites lutea, growing on and off metal-polluted sites. Plant Biol. 11:170–78 [Google Scholar]
  85. Losner-Goshen D, Portnoy VH, Mayer AM, Joel DM. 85.  1998. Pectolytic activity by the haustorium of the parasitic plant Orobanche L. (Orobanchaceae) in host roots. Ann. Bot. 81:319–26 [Google Scholar]
  86. Matvienko M, Torres MJ, Yoder JI. 86.  2001. Transcriptional responses in the hemiparasitic plant Triphysaria versicolor to host plant signals. Plant Physiol. 127:272–82 [Google Scholar]
  87. Matvienko M, Wojtowicz A, Wrobel R, Jamison D, Goldwasser Y, Yoder JI. 87.  2001. Quinone oxidoreductase message levels are differentially regulated in parasitic and non-parasitic plants exposed to allelopathic quinones. Plant J. 25:375–87 [Google Scholar]
  88. Mendgen K, Hahn M. 88.  2002. Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7:352–56 [Google Scholar]
  89. Mitsumasu K, Seto Y, Yoshida S. 89.  2015. Apoplastic interactions between plants and plant root intruders. Front. Plant Sci. 6:617 [Google Scholar]
  90. Musselman LJ, Dickison WC. 90.  1975. The structure and development of the haustorium in parasitic Scrophulariaceae. Bot. J. Linn. Soc. 70:183–212 [Google Scholar]
  91. Mutuku JM, Yoshida S, Shimizu T, Ichihashi Y, Wakatake T. 91.  et al. 2015. The WRKY45-dependent signaling pathway is required for resistance against Striga hermonthica parasitism. Plant Physiol. 168:1152–63 [Google Scholar]
  92. Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N. 92.  2012. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. PNAS 109:10101–6 [Google Scholar]
  93. Naumann J, Salomo K, Der JP, Wafula EK, Bolin JF. 93.  et al. 2013. Single-copy nuclear genes place haustorial Hydnoraceae within Piperales and reveal a cretaceous origin of multiple parasitic angiosperm lineages. PLOS ONE 8:e79204 [Google Scholar]
  94. Neumann U, Salle G, Weber HC. 94.  1998. Development and structure of the haustorium of the parasite Rhamphicarpa fistulosa (Scrophulariaceae). Bot. Acta 111:354–65 [Google Scholar]
  95. Neumann U, Vian B, Weber HC, Salle G. 95.  1999. Interface between haustoria of parasitic members of the Scrophulariaceae and their hosts: a histochemical and immunocytochemical approach. Protoplasma 207:84–97 [Google Scholar]
  96. Nikolov LA, Staedler YM, Manickam S, Schonenberger J, Endress PK. 96.  et al. 2014. Floral structure and development in Rafflesiaceae with emphasis on their exceptional gynoecia. Am. J. Bot. 101:225–43 [Google Scholar]
  97. Nikolov LA, Tomlinson PB, Manickam S, Endress PK, Kramer EM, Davis CC. 97.  2014. Holoparasitic Rafflesiaceae possess the most reduced endophytes and yet give rise to the world's largest flowers. Ann. Bot. 114:233–42 [Google Scholar]
  98. Nowara D, Gay A, Lacomme C, Shaw J, Ridout C. 98.  et al. 2010. HIGS: host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell 22:3130–41 [Google Scholar]
  99. Nwoke FIO. 99.  1982. The initiation of the secondary haustorium in Alectra vogelii Benth. Ann. Bot. 49:669–76 [Google Scholar]
  100. O'Malley RC, Lynn DG. 100.  2000. Expansin message regulation in parasitic angiosperms: marking time in development. Plant Cell 12:1455–65 [Google Scholar]
  101. Okamoto S, Shinohara H, Mori T, Matsubayashi Y, Kawaguchi M. 101.  2013. Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4:2191 [Google Scholar]
  102. Olivier A, Benhamou N, Leroux GD. 102.  1991. Cell surface interactions between sorghum roots and the parasitic weed Striga hermonthica: cytochemical aspects of cellulose distribution in resistant and susceptible host tissues. Can. J. Bot. 69:1679–90 [Google Scholar]
  103. Ouedraogo O, Neumann U, Raynal-Roques A, Salle G, Tuquet C, Dembele B. 103.  1999. New insights concerning the ecology and the biology of Rhamphicarpa fistulosa (Scrophulariaceae). Weed Res. 39:159–69 [Google Scholar]
  104. Parker C. 104.  2009. Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag. Sci. 65:453–59 [Google Scholar]
  105. Pérez-de-Luque A. 105.  2013. Haustorium invasion into host tissues. See Ref. 68 75–86
  106. Perret X, Staehelin C, Broughton WJ. 106.  2000. Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64:180–201 [Google Scholar]
  107. Petrasek J, Friml J. 107.  2009. Auxin transport routes in plant development. Development 136:2675–88 [Google Scholar]
  108. Pielach A, Leroux O, Domozych DS, Knox JP, Popper ZA. 108.  2014. Arabinogalactan protein-rich cell walls, paramural deposits and ergastic globules define the hyaline bodies of rhinanthoid Orobanchaceae haustoria. Ann. Bot. 114:1359–73 [Google Scholar]
  109. Ranjan A, Ichihashi Y, Farhi M, Zumstein K, Townsley B. 109.  et al. 2014. De novo assembly and characterization of the transcriptome of the parasitic weed Cuscuta pentagona identifies genes associated with plant parasitism. Plant Physiol. 166:1186–99 [Google Scholar]
  110. Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV. 110.  et al. 2013. Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342:1468–73 [Google Scholar]
  111. Riopel JL. 111.  1979. Experimental studies on induction of haustoria in Agalinis purpurea. In Proceedings of the Second Symposium on Parasitic Weeds LJ Musselman, AD Worsham, RE Eplee 165–73 Raleigh: N.C. State Univ. [Google Scholar]
  112. Riopel JL, Timko MP. 112.  1995. Haustorial initiation and differentiation. Parasitic Plants MC Press, JD Graves 39–79 New York: Chapman & Hall [Google Scholar]
  113. Robert S, Simier P, Fer A. 113.  1999. Purification and characterization of mannose 6-phosphate reductase, a potential target for the control of Striga hermonthica and Orobanche ramosa. Funct. Plant Biol. 26:233–37 [Google Scholar]
  114. Roney JK, Khatibi PA, Westwood JH. 114.  2007. Cross-species translocation of mRNA from host plants into the parasitic plant dodder. Plant Physiol. 143:1037–43 [Google Scholar]
  115. Runyon JB, Mescher MC, De Moraes CM. 115.  2006. Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–67 [Google Scholar]
  116. Runyon JB, Mescher MC, Felton GW, De Moraes CM. 116.  2010. Parasitism by Cuscuta pentagona sequentially induces JA and SA defence pathways in tomato. Plant Cell Environ. 33:290–303 [Google Scholar]
  117. Sanchez-Puerta MV. 117.  2014. Involvement of plastid, mitochondrial and nuclear genomes in plant-to-plant horizontal gene transfer. Acta Soc. Bot. Pol. 83:317–23 [Google Scholar]
  118. Scholes JD, Press MC. 118.  2008. Striga infestation of cereal crops—an unsolved problem in resource limited agriculture. Curr. Opin. Plant Biol. 11:180–86 [Google Scholar]
  119. Smith CE, Dudley MW, Lynn DG. 119.  1990. Vegetative/parasitic transition: control and plasticity in Striga development. Plant Physiol. 93:208–15 [Google Scholar]
  120. Smith CE, Ruttledge T, Zeng Z, O'Malley RC, Lynn DG. 120.  1996. A mechanism for inducing plant development: the genesis of a specific inhibitor. PNAS 93:6986–91 [Google Scholar]
  121. Smith JD, Mescher MC, De Moraes CM. 121.  2013. Implications of bioactive solute transfer from hosts to parasitic plants. Curr. Opin. Plant Biol. 16:464–72 [Google Scholar]
  122. Smith S, Stewart GR. 122.  1990. Effect of potassium levels on the stomatal behavior of the hemi-parasite Striga hermonthica. Plant Physiol. 94:1472–76 [Google Scholar]
  123. Spallek T, Mutuku M, Shirasu K. 123.  2013. The genus Striga: a witch profile. Mol. Plant Pathol. 14:861–69 [Google Scholar]
  124. Sparla F, Tedeschi G, Trost P. 124.  1996. NAD(P)H:(quinone-acceptor) oxidoreductase of tobacco leaves is a flavin mononucleotide-containing flavoenzyme. Plant Physiol. 112:249–58 [Google Scholar]
  125. Suetsugu K, Kawakita A, Kato M. 125.  2008. Host range and selectivity of the hemiparasitic plant Thesium chinense (Santalaceae). Ann. Bot. 102:49–55 [Google Scholar]
  126. Swarbrick PJ, Huang K, Liu G, Slate J, Press MC, Scholes JD. 126.  2008. Global patterns of gene expression in rice cultivars undergoing a susceptible or resistant interaction with the parasitic plant Striga hermonthica. New Phytol. 179:515–29 [Google Scholar]
  127. Swarup K, Benkova E, Swarup R, Casimiro I, Peret B. 127.  et al. 2008. The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10:946–54 [Google Scholar]
  128. Tennakoon KU, Cameron DD. 128.  2006. The anatomy of Santalum album (Sandalwood) haustoria. Can. J. Bot. 84:1608–16 [Google Scholar]
  129. Tesitel J, Tesitelova T, Fisher JP, Leps J, Cameron DD. 129.  2015. Integrating ecology and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources shape the interplay between parasitism and autotrophy. New Phytol. 205:350–60 [Google Scholar]
  130. Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W. 130.  et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 1:15025 [Google Scholar]
  131. Toh S, Holbrook-Smith D, Stogios PJ, Onopriyenko O, Lumba S. 131.  et al. 2015. Structure-function analysis identifies highly sensitive strigolactone receptors in Striga. Science 350:203–7 [Google Scholar]
  132. Tomilov AA, Tomilova NB, Abdallah I, Yoder JI. 132.  2005. Localized hormone fluxes and early haustorium development in the hemiparasitic plant Triphysaria versicolor. Plant Physiol. 138:1469–80 [Google Scholar]
  133. Tomilov AA, Tomilova NB, Wroblewski T, Michelmore R, Yoder JI. 133.  2008. Trans-specific gene silencing between host and parasitic plants. Plant J. 56:389–97 [Google Scholar]
  134. Tomilov AA, Tomilova NB, Yoder JI. 134.  2006. Agrobacterium tumefaciens and Agrobacterium rhizogenes transformed roots of the parasitic plant Triphysaria versicolor retain parasitic competence. Planta 225:1059–71 [Google Scholar]
  135. Tsuchiya Y, Yoshimura M, Sato Y, Kuwata K, Toh S. 135.  et al. 2015. Probing strigolactone receptors in Striga hermonthica with fluorescence. Science 349:864–68 [Google Scholar]
  136. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T. 136.  et al. 2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200 [Google Scholar]
  137. Vaughn KC. 137.  2002. Attachment of the parasitic weed dodder to the host. Protoplasma 219:227–37 [Google Scholar]
  138. Vaughn KC. 138.  2003. Dodder hyphae invade the host: a structural and immunocytochemical characterization. Protoplasma 220:189–200 [Google Scholar]
  139. Vaughn KC. 139.  2006. Conversion of the searching hyphae of dodder intoxylic and phloic hyphae: a cytochemical and immunocytochemical investigation. Int. J. Plant Sci. 167:1099–114 [Google Scholar]
  140. Visser JH, Dorr I, Kollmann R. 140.  1984. The “hyaline body” of the root parasite Alectra orobanchoides benth. (Scrophulariaceae)—its anatomy, ultrastructure and histochemistry. Protoplasma 121:146–56 [Google Scholar]
  141. Weber HC. 141.  1987. Evolution of the secondary haustoria to a primary haustorium in the parasitic Scrophulariaceae-Orobanchaceae. Plant Syst. Evol. 156:127–31 [Google Scholar]
  142. Westwood JH, dePamphilis CW, Das M, Fernández-Aparicio M, Honaas LA. 142.  et al. 2011. The Parasitic Plant Genome Project: new tools for understanding the biology of Orobanche and Striga. Weed Sci. 60:295–306 [Google Scholar]
  143. Westwood JH, Yoder JI, Timko MP, dePamphilis CW. 143.  2010. The evolution of parasitism in plants. Trends Plant Sci. 15:227–35 [Google Scholar]
  144. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K. 144.  et al. 2012. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb. Symp. Quant. Biol. 77:235–47 [Google Scholar]
  145. Wing RA, Yamaguchi J, Larabell SK, Ursin VM, McCormick S. 145.  1990. Molecular and genetic characterization of two pollen-expressed genes that have sequence similarity to pectate lyases of the plant pathogen Erwinia. Plant Mol. Biol. 14:17–28 [Google Scholar]
  146. Xi Z, Bradley RK, Wurdack KJ, Wong K, Sugumaran M. 146.  et al. 2012. Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genom. 13:227 [Google Scholar]
  147. Xi Z, Wang Y, Bradley RK, Sugumaran M, Marx CJ. 147.  et al. 2013. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLOS Genet. 9:e1003265 [Google Scholar]
  148. Yang Z, Wafula EK, Honaas LA, Zhang H, Das M. 148.  et al. 2015. Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty. Mol. Biol. Evol. 32:767–90Identified potentially common haustorium genes from the Orobanchaceae and predicted their evolutionary origin. [Google Scholar]
  149. Yoshida S, Kim S, Wafula EK, Tanskanen J, Kim Y-M. 149.  et al. 2016. Genome sequence of Striga asiatica provides insight into the evolution of plant parasitism. Submitted Presents the first complete genome sequencing of the parasitic plant S. asiatica.
  150. Yoshida S, Maruyama S, Nozaki H, Shirasu K. 150.  2010. Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 328:1128Presented evidence of nuclear gene transfer from hosts to parasites. [Google Scholar]
  151. Yoshida S, Shirasu K. 151.  2009. Multiple layers of incompatibility to the parasitic witchweed, Striga hermonthica. New Phytol. 183:180–89 [Google Scholar]
  152. Yoshida S, Shirasu K. 152.  2012. Plants that attack plants: molecular elucidation of plant parasitism. Curr. Opin. Plant Biol. 15:708–13 [Google Scholar]
  153. Zhang D, Qi J, Yue J, Huang J, Sun T. 153.  et al. 2014. Root parasitic plant Orobanche aegyptiaca and shoot parasitic plant Cuscuta australis obtained genes by horizontal gene transfer. BMC Plant Biol. 14:19 [Google Scholar]
  154. Zhang Y, Fernandez-Aparicio M, Wafula EK, Das M, Jiao Y. 154.  et al. 2013. Evolution of a horizontally acquired legume gene, albumin 1, in the parasitic plant Phelipanche aegyptiaca and related species. BMC Evol. Biol. 13:48 [Google Scholar]
  155. Zhou WJ, Yoneyama K, Takeuchi Y, Iso S, Rungmekarat S. 155.  et al. 2004. In vitro infection of host roots by differentiated calli of the parasitic plant Orobanche. J. Exp. Bot. 55:899–907 [Google Scholar]
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